Hugo Cayuela

To breed or not to breed: past reproductive status and environmental cues drive current breeding decisions in a long-lived amphibian

Iteroparity is an adaptive response to uncertainty in reproductive success. However, spreading reproductive success over multiple reproduction events during a lifetime is constrained by adult mortality and the stochasticity associated with interactions between external factors and physiological states. The acquisition of information about environmental conditions during the growth of progeny and sufficient resources during the non-reproductive period are key factors for breeding success. Consequently, we hypothesized that long-lived animals may skip a breeding opportunity when information about unfavourable environmental conditions is available. In addition, nutritional constraints could prevent an animal from replenishing its reserves sufficiently to invest in the current breeding period. We investigated these questions using capture–recapture data from a 5-year study on a large population of yellow-bellied toads in a forest in north-eastern France. We took advantage of various advances in multi-state capture–recapture models (e.g. unobservable states and mixture models) to test our hypotheses. Our results show that the combined effects of rainfall deficit and the breeding/non-breeding state of individuals during the past breeding season affect breeding probability during the following breeding opportunity. We also found that females breed less frequently than males, suggesting that the overall energy cost of reproduction differs between genders. Finally, the results indicate that toad survival appears to be negatively influenced by rainfall deficits. We discuss the yellow-bellied toad’s reproductive behaviour in term of bet-hedging strategy and life history trait evolution.

The best of a harsh lot in a specialized species: breeding habitat use by the yellow-bellied toad (Bombina variegata) on rocky riverbanks

Because of the narrowness of their niches, specialised species are often vulnerable because their populations suffer from fragmentation or low densities. Whatever the causes of their specialization, one might expect micro-habitat selection to be strong within the boundaries of the chosen niche to compensate for the costs linked to habitat constraints (variability of reproductive success due to high larval mortality, habitat fragmentation). We tested this hypothesis by investigating breeding site selection in the yellow-bellied toad (Bombina variegata) in the context of rock pools at riverbanks, which are supposed to be one of the pristine habitats of the species. In this species, breeding habitat use differs markedly from that of other European anurans since spawning takes place in small pools located in the close vicinity of rivers. Such pools experience high risks of drying up and flooding. By measuring 8 habitat variables at 187 rock pools along a 250 m river segment, we show a breeding habitat use based on a preference for pools with large volumes of water provided that they are devoid of alluvia, with a good exposition to sun. By ensuring longer water periods and faster development rates, large volumes and warm water probably reduce the mortality risks due to drying up (within suitable temperature range). This result contributes to understanding the process of niche conservatism (persistence of narrow range on certain dimensions of the niche), which is an important challenge in ecology and conservation biology.

Contrasting patterns of environmental fluctuation contribute to divergent life histories among amphibian populations

Because it modulates the fitness returns of possible options of energy expenditure at each ontogenetic stage, environmental stochasticity is usually considered a selective force in driving or constraining possible life histories. Divergent regimes of environmental fluctuation experienced by populations are expected to generate differences in the resource allocation schedule between survival and reproductive effort and outputs. To our knowledge, no study has previously examined how different regimes of stochastic variation in environmental conditions could result in changes in both the temporal variation and mean of demographic parameters, which could then lead to intraspecific variation along the slow-fast continuum of life history tactics. To investigate these issues, we used capture-recapture data collected on five populations of a long-lived amphibian (Bombina variegata) experiencing two distinct levels of stochastic environmental variation: (1) constant availability of breeding sites in space and time (predictable environment), and (2) variable spatio-temporal availability of breeding sites (unpredictable environment). We found that female breeding propensity varied more from year to year in unpredictable than in predictable environments. Although females in unpredictable environments produced on average more viable offspring per year, offspring production was more variable between years. Survival at each ontogenetic stage was slightly lower and varied significantly more from year to year in unpredictable environments. Taken together, these results confirm that increased environmental stochasticity can modify the resource allocation schedule between survival and reproductive effort and outputs and may lead to intraspecific variation along the slow-fast continuum of life history tactics.

Demographic responses to weather fluctuations are context dependent in a long-lived amphibian.

Weather fluctuations have been demonstrated to affect demographic traits in many species. In long-lived organisms, their impact on adult survival might be buffered by the evolution of traits that reduce variation in interannual adult survival. For example, skipping breeding is an effective behavioral mechanism that may limit yearly variation in adult survival when harsh weather conditions occur; however, this in turn would likely lead to strong variation in recruitment. Yet, only a few studies to date have examined the impact of weather variation on survival, recruitment and breeding probability simultaneously in different populations of the same species. To fill this gap, we studied the impact of spring temperatures and spring rainfall on survival, on reproductive skipping behavior and on recruitment in five populations of a long-lived amphibian, the yellow-bellied toad (Bombina variegata). Based on capture-recapture data, our findings demonstrate that survival depends on interactions between age, population and weather variation. Varying weather conditions in the spring result in strong variation in the survival of immature toads, whereas they have little effect on adult toads. Breeding probability depends on both the individuals previous reproductive status and on the weather conditions during the current breeding season, leading to high interannual variation in recruitment. Crucially, we found that the impact of weather variation on demographic traits is largely context dependent and may thus differ sharply between populations. Our results suggest that studies predicting the impact of climate change on population dynamics should be taken with caution when the relationship between climate and demographic traits is established using only one population or few populations. We therefore highly recommend further research that includes surveys replicated in a substantial number of populations to account for context-dependent variation in demographic processes.

Females trade off the uncertainty of breeding resource suitability with male quality during mate choice in an anuran

In many species, females may be particularly selective about the expected direct benefits of choosing a potential mate or the males genetic contribution to their offspring. Growing evidence suggests that female choosiness can also be influenced, for instance, by local abiotic factors, the social environment or the presence of heterospecifics. In amphibians that breed in highly temporary ponds with limited trophic resources (such as the yellow-bellied toad, Bombina variegata), competition during larval development may have a strong impact on the fitness of offspring. Accordingly, one might expect females to apply hierarchical decision making, balancing intraspecific competition risks during larval growth against the relative indirect benefits associated with the quality of the male. To investigate this issue, we conducted experiments in seminatural enclosures to test whether the preference of yellow-bellied toad females for good call attractiveness (determined by fundamental frequency) is affected by the risk of larval competition within the pond occupied by the callers. Overall, our results showed that females have a preference for low-frequency calls when prior information does not enable them to assess the relative quality of ponds. However, when prior information enables females to unambiguously determine relative pond quality, females appear to apply hierarchical decision making in which the quality of a pond prevails over call cues related to the quality of the male.

Is the exotic red swamp crayfish (Procambarus clarkii) a current threat for the Mediterranean tree frog (Hyla meridionalis) in the Camargue (Southern France)

The non-indigenous red swamp crayfish (Procambarus clarkii) has been shown to be a threat for amphibian conservation. Many amphibian species breed in temporary ponds to diminish predation risk as such ecosystems are free of large predators. However P. clarkii, occurring as an invasive species in the Camargue delta, can readily disperse on the ground and thus colonize isolated ponds. We studied the current impact of the exotic crayfish on the reproductive success of the Mediterranean tree frog (Hyla meridionalis). In a mesocosm experiment, we tested the effect of two crayfish densities (1 and 3 crayfish/m2) on tadpole abundance. We also tested in a field experiment, within a temporary pond, the crayfish’s predation on the tree frog’s eggs. Finally, we developed site occupancy models using data from 20 ponds to assess the effect of crayfish abundance on tadpole abundance. Neither the experiments, nor the site occupancy models showed a negative impact of the current crayfish abundance on the tree frog populations breeding in ponds. We found that recorded crayfish densities were lower than in other areas where crayfish has impacted amphibian populations, but we hypothesize that current crayfish abundance in the area may increase in the future, thus impacting tree frog populations.

Dispersal and alternative breeding site fidelity strategies in an amphibian

Dispersal (i.e. movement from a natal or breeding site to another breeding site) is a central process in ecology and evolution as it affects the eco-evolutionary dynamics of spatially structured populations. Dispersal evolution is regulated by the balance between costs and benefits, which is influenced by the individual phenotype (i.e. phenotype-dependent dispersal) and environmental factors (i.e. condition-dependent dispersal). Even though these processes have been extensively studied in species with simple life cycles, our knowledge about these mechanisms in organisms displaying complex life cycles remains fragmentary. In fact, little is specifically known about how the interplay between individual and environmental factors may lead to alternative dispersal strategies that, in turn, lead to the coexistence of contrasted site fidelity phenotypes. In this paper, we examined breeding dispersal in a pond-breeding amphibian, the great crested newt Triturus cristatus, within usual walking distances for a newt. We took advantage of recent developments in multi-event capture–recapture models and used capture–recapture data (946 newts marked) collected in a spatially structured population occupying a large pond network (73 ponds). We showed a high rate of breeding site infidelity (i.e. pond use) and the coexistence of two dispersal phenotypes, namely, a highly pond faithful phenotype and a dispersing phenotype. Individuals that were site faithful at time t – 1 were therefore more likely to remain site faithful at time t. Our results also demonstrated that the probability that individuals belong to one or the other dispersal phenotypes depended on environmental and individual factors. In particular, we highlighted the existence of a dispersal syndrome implying a covariation pattern among dispersal behavior, body size, and survival. Our work opens new research prospects in the evolution of dispersal in organisms displaying complex life cycles and raises interesting questions about the evolutionary pathways that contribute to the diversification of movement strategies in the wild.

Intensive vehicle traffic impacts morphology and endocrine stress response in a threatened amphibian

Amphibians are considered to be the most threa- tened group of vertebrates. Among the multiple factors in- volved in their decline, habitat loss and alteration as a result of human activities is a major threat. At the individual level the effects of habitat alteration are potentially multiple, in- cluding a range of morphological and physiological re- sponses. Analysing and understanding these responses is therefore a critical challenge for amphibian conservation. We examined the influence of intensive vehicle traffic (mo- torbikes and trucks on unpaved pathways) on the body size and condition and on the production of glucocorticoids (i.e. corticosterone) in the yellow-bellied toad Bombina variegata. In particular, we tested the hypothesis that intensive vehicle traffic has a negative influence on body size and body con- dition, and postulated that it also increases corticosterone production. Using morphometric data and saliva samples collected from four populations in France, we found that intensive vehicle traffic is associated with a decrease in body size and body condition in both males and females. Furthermore, our analysis revealed that corticosterone pro- duction was lower in both sexes in populations experiencing intensive vehicle traffic. We suggest that measures should be applied to reduce vehicle traffic intensity on unpaved pathways during toad breeding activity. This is critical for B. variegata, for which man-made ruts and residual puddles could mitigate the loss of natural habitats.

Toads and roads: transport infrastructure severely impacts dispersal regardless of life stage

Transport infrastructure such as roads has been reported to negatively affect dispersal. Their effects on dispersal are thought to be complex, depending on the characteristics of the structure and the intensity of the traffic using it. In addition, individual factors, such as age, may strongly affect dispersal decisions and success when individuals are confronted with transport infrastructure. Despite the importance of this topic for wildlife conservation, few studies have investigated the effect of transport infrastructure on individuals’ dispersal decisions before and after sexual maturity. We examined the effects on two kinds of infrastructure, gravel tracks and paved roads, on the dispersal of an endangered amphibian, the yellow-bellied toad (Bombina variegata). We used capture-recapture data collected during a five-year period on a large, spatially structured population of B. variegata. Our study revealed that emigration rates increased with an individual’s age, while dispersal distance decreased. It also showed that both tracks and roads had negative effects on dispersal. The negative effect of roads was stronger than that of tracks. We additionally found that the effect of tracks on dispersal slightly decreased with a toad’s age. In contrast, the negative effect of roads was severe and relatively similar across age classes.

Survival cost to relocation does not reduce population self-sustainability in an amphibian

Relocations are increasingly popular among wildlife managers despite sharp debate and low rate of relocation success in vertebrates. In this context, understanding the influence of extrinsic (e.g., relocation design, habitat characteristics) and intrinsic factors (e.g., age and sex) on demographic parameters such as survival that regulate the dynamics of relocated populations is critical to improve relocation protocols and better predict relocation success. We investigated survival in naturally established and relocated populations of yellow-bellied toads (Bombina variegata), an amphibian that was nearly extinct in Belgium by the late 1990s. We quantified survival at three ontogenetic stages (juvenile, subadult, and adult) in the relocated population, the source population, and a control population. In the relocated population, we quantified survival in captive bred individuals and their locally born descendants. We showed that survival at juvenile and subadult stages was relatively similar in all populations. In contrast, relocated adult survival was lower than adult survival in the source and control populations. Despite this, offspring of relocated animals (the next generation, regardless of life stage) survived at similar rates to offspring in the source and control populations. Our simulations revealed that the relocated population was self-sustaining under different scenarios and that the fate (e.g., stability or finite rate of increase) of the simulated populations was highly dependent on the fecundity of relocated adults and their offspring. Policy implications. Our results indicate that survival in relocated individuals is lower than in non-relocated individuals but that this cost (= reduced survival) disappears in the second generation. A finer understanding of how relocation affects demographic processes is an important step in improving relocation success of amphibians and other animals.